It
is well known that the sex in mammals is determined by the X and Y chromosomes,
the XY being male and the XX being female, whereas the sex in birds is determined
by the Z and W chromosomes (ZZ males and ZW females). These XY and ZW systems
have a history of about 200 million years. Therefore, the sex determination
system seems to be quite stable once it is established (1).
In
amphibians, however, this is not the case, and the same taxonomic family may
include species with both the XY and ZW systems (2). In an extreme case the
same species contains both the XY and ZW systems as polymorphism. This
situation is observed in the Japanese frog Rana
rugosa. This species inhabits almost the entire territory of Japan, but
depending on the geographical area the chromosomal system is either the XY or
the ZW (see Fig. 1). The ZW system is heterogametic, and therefore the male and
female can be distinguished by the chromosomal morphology. However, the XY
system is either heterogametic (Hamakita areas) or homogametic (Hiroshima and Isehara
areas) depending on the geographical area (3). Further studies have shown that
the gene sequence arrangements of the X and Y chromosomes from Hiroshima and
Isehara are different from each other (Fig. 1). How did these chromosomal
systems evolve? Solution of this question may allow us to understand the
general scheme of evolution of sex determination.
Miura
et al. (3) studied the evolutionary history of these sex chromosomes by using
the sex-linked gene, AP/ATP translocase gene,
on the sex chromosome (chromosome 7). The phylogenetic tree constructed from
this gene is presented in Fig. 2. On the basis of this phylogenetic tree, they
proposed the evolutionary scenario presented in Fig. 3. This scenario suggests
that the “subtelocentric chromosomes” in the Hiroshima area first generated the
“more subtelocentric chromosomes” similar to the chromosomes from the Isehara
area. The parental “subtelocentric chromosomes” are then hybridized with the “more
subtelocentric chromosomes” to produce the “metacentric chromosomes.” Finally,
these “metacentric chromosomes” and the Hiroshima “subtelocentric chromosomes”
generated the XY and the ZW chromosomal systems. These evolutionary changes are
believed to have occurred relatively recently.
However,
there are several problems in this scenario. The first and most important one,
which the authors also recognized, is the nature and the location of
sex-determining genes on the sex chromosomes. The sex is determined not by
chromosomes but by genes, and therefore it is essential to identify the genes
that trigger the formation of testis or ovary. Chromosomal morphology can
change relatively easily by inversion and translocation, but the
sex-determining genes are generally more conserved, and therefore they are
likely to give a more accurate pattern of evolution of sex determination.
Furthermore, the morphological study of chromosomes does not give information
on small gene deletions, insertions, or pseudonization. It is therefore
difficult to reconstruct the evolutionary history of sex determination in the
present case.
For
the above reason, the authors have not clearly distinguished between the X and
Y chromosomes in the Hiroshima and Isehara areas (Fig. 1 and 3). Fig. 2,
however, indicates that the X and W chromosomes and the Y and Z chromosomes are
evolutionarily related, respectively. Although the phylogenetic tree was
constructed by using a sex-linked gene rather than the sex determining gene,
the results presented are interesting if we consider the mammalian sex determining
gene, SRY, that initiates the pathway
of testis formation. In this case the individual without the SRY gene becomes female as a default
option. In birds, which have the ZW system, the male (ZZ) is believed to form
testis because of the presence of two copies of the sex determining gene, Dmrt1, and the ZW female produces ovary
as a default option (2, 4).
At
the present time we know nothing about the molecular basis of sex determination
in frogs. However, if we use the sex determination in mammals and birds as
guidance, the evolutionary changes of the XY and ZW systems may be studied at
the molecular level.
In
this connection, Miura et al. (5) presented an interesting observation with
respect to the accumulation of lethal mutations in the Y and W chromosomes. In
frogs it is possible to generate the WW homozygotes by producing the ZW males with
a hormone treatment and by crossing the ZW males with the normal ZW females (5).
This WW homozygote did not survive well in the tadpole stage, and most of the
individuals died sooner or later. When the WW homozygotes were produced from
various geographical locations, it was clear that the W chromosome carries a
lethal mutation but the lethal mutation varies from location to location. In
other words, the W chromosome evolved independently in different locations. Therefore,
when the WW was produced by using the W chromosome from different locations,
the WW homozygotes could survive up to adulthood.
The
same type of experiment was done with the Y chromosome. In this case the YY
individual could not survive even if the two different Y’s were derived from
different locations. This suggests that the XY system evolved earlier than the
ZW system.
It
has been argued that once a set of linked genes related to sex determination
evolve in a chromosome the recombination value of the linked gene region tends
to be reduced by modifier genes (6) or chromosomal inversions (7) and the
recessive lethal mutations gradually accumulate in the region (8, 9). The rate
of accumulation of lethal mutations depends on the mutation rate, population
size, and evolutionary time.
The
evolutionary change between the XY and ZW systems also occurs more frequently
in small populations than in large populations. Because the R. rugosa frogs generally inhabit the mountainous
areas, the effective population size must be very small. Probably for these
reasons, R. rugosa have undergone
rather rapid changes of the sex chromosome (chromosome 7) and the genes
controlling sex determination. However, the evolutionary changes of sex
determining genes are poorly understood at present. It is hoped that a more
detailed molecular study will be conducted for understanding the evolutionary mechanism
of sex determination in the future.
References
1. Graves JAM. 2008. Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Ann Rev Genet 42:565-586.
2. Sarre SD, Ezaz T, and Georges A.
2011. Transitions between sex-determining systems in reptiles and amphibians.
Annu Rev Genomics Hum Genet 12:391-406.
3.
Miura I, Ohtani H, Nakamura M, Ichikawa Y, and Saitoh K. 1998. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, Inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol Biol Evol
15(12):1612-1619.
4.
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM,
Farlie PG, Doran TJ, and & Sinclair AH. 2009. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267-271.
5.
Miura I, Ohtani H, and Ogata M. 2012. Independent degeneration of W and Y sex chromosomes in frog Rana rugosa.Chromosome Res 20:47-55.
6.
Nei, M. 1969. Linkage modification and sex difference in recombination. Genetics 63:681-699.
7.
Ohno S. 1967. Sex chromosomes and sex-linked genes. Springer-Verlag, New York.
8. Muller HJ. 1914. A gene for the fourth chromosome of Drosophila. J Exp Zool 17:325-336.
9. Nei, M. 1970. Accumulation of nonfunctional genes on sheltered chromosomes. Am. Nat. 104:311-322.
No comments:
Post a Comment